Trees (2011) 25:133144 DOI 10.

1007/s00468-010-0529-3

ORIGINAL PAPER

Dendrochronology of lianas of the Leguminosae family from the Atlantic Forest, Brazil
Arno Fritz Neves Brandes Claudio Sergio Lisi Claudia Franca Barros

Received: 1 November 2010 / Revised: 30 November 2010 / Accepted: 3 December 2010 / Published online: 29 December 2010 Springer-Verlag 2010

Abstract Information about plant growth, development and age forms the basis for understanding complex forest ecological processes. Although lianas play an important role in tropical forests, little is known about their growth and development from either climatic or ecological perspectives. Therefore, we studied the growth rings in Legume liana species collected in a mountainous Atlantic Forest in southeastern Brazil. Four of the eight studied species did not show cambial variants, three had a lobed stem, and one had a furrowed xylem. Distinct growth rings were observed in all species. Semi-ring porosity, marginal parenchyma, brous zone and radially attened latewood cells were the main characteristic features of these growth rings. Species without cambial variants, including Dalbergia frutescens, Piptadenia adiantoides, P. micracantha and Senegalia tenuifolia, showed very distinct growth rings visible in macroscopic and microscopic analysis. Ring-width time series and cambial wound assessment were performed to analyze periodicity and dendrochronology. The species with cambial variants, S. grandistipula,

S. lacerans, S. martiusiana and S. pedicellata, also showed distinct growth rings, however, sometimes barely detectable or not detected at all. Cambial wounding, cross-dating and climate-growth relationships indicated the annual nature of growth rings in species without cambial variant. Crossdating between radii within one individual and between individuals was successful, and the synchronized series enabled us to build species chronologies and a mean chronology. Climate-growth analysis revealed signicant correlations between chronologies and precipitation, indicating that available moisture is the main factor determining growth rates of lianas in the Atlantic forest. Keywords Lianas Tropics Wood anatomy Cambial variants Dendroecology Growth rings Leguminosae

Introduction Lianas are an essential component of tropical forest ecosystems. As such, lianas represent about 25% of the abundance and species richness (Gentry 1991; Perez-Salicrup et al. 2004; Schnitzer and Bongers 2002). During the past two decades awareness and interest in this growth form have increased. However, in many respects, lianas are still poorly understood, particularly liana ecology at the species level and the response of lianas to the environment (Gerwing 2004; Isnard and Silk 2009). In addition, little attention has been given to the anatomy of lianas (Bamber and Ter Welle 1994) and to the analysis of growth rings, although a few older reports do exist (e.g., Schenck 1893). So far, dendrochronological studies on lianas were developed only in temperate climate regions, especially with Hedera helix (Gar and Ficarrotta 2003; Heuze et al. 2009; Nola 1997; Schnitzler and Heuze 2006; Verheyden et al.

Communicated by A. Braeuning. Contribution to the special issueTropical Dendroecology. A. F. N. Brandes (&) C. F. Barros Instituto de Pesquisas Jardim Botanico do Rio de Janeiro, Diretoria de Pesquisas, Laboratorio de Botanica Estrutural, Rua Pacheco Leao 915, Jardim Botanico, Rio de Janeiro, RJ 22460-030, Brazil e-mail: arnofnb@jbrj.gov.br C. S. Lisi Departamento de Biologia, CCBS, Universidade Federal de Sergipe, Av. Marechal Rondon s/n, Rosa Elze, Sao Cristovao, SE 49100-000, Brazil e-mail: arnofnb@jbrj.gov.br

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2006), which have improved our understanding of liana host interactions and climategrowth relationships of liana species. Another notable growth ring analysis in lianas was done at the beginning of the twentieth century, and it reported the estimated age in Clematis vitalba L. (Kanngiesser 1906 apud Schweingruber and Poschlod 2005). Information about growth rings in trees is available, but it is scarce for other growth forms. Schweingruber and Poschlod (2005) studied growth rings in herbs and shrubs, proving the great value of dendrochronology for the temporal understanding of other growth forms and for ecological studies. Nonetheless, studies reporting the growth and age of lianas are sparse, and they are mostly restricted to indirect methods (Ewers et al. 1991; Gerwing 2004; Nabe-Nielsen 2002; Putz 1990). Therefore, dendrochronology may be a valuable tool in future research with lianas. Specically, growth ring analysis can contribute chronological information that can be used for growth analysis, wood production, population age structure and forest dynamics, lianahost interaction, forest management, as well as conservation and restoration studies (Braker 2002; Brienen and Zuidema 2006; Eckstein et al. 1995; Grau et al. 2003; Jacoby 1989; Nola 1997; Priya and Bhat 1999; Worbes 2002; Worbes et al. 2003). Still, these analyses can only be performed for lianas if anatomical and dendrochronological studies are also performed. In the past few decades, many dendrochronological studies of tropical tree species have reported the occurrence of seasonal growth rings that are correlated, in many cases, with precipitation or some other seasonal climatic variations (Baas and Vetter 1989; Bormann and Berlym 1981; Eckstein and Baas 1999; Eckstein et al. 1995). In Brazil, some studies were developed in the Amazon Forest (Botosso 1984; Schongart et al. 2005; Schongart 2008; Vetter and Botosso 1989; Worbes 1985, 1989) and the Atlantic Forest biomes (Callado et al. 2001a, b, 2004; Estrada et al. 2008; Lisi et al. 2008; Oliveira et al. 2009, 2010; Seitz and Kanninen 1989). These studies and others showed the viability of growth ring research in the tropics, and an excellent thematic overview was presented by Worbes (2002). Lianas are woody climbers whose development begins on the ground. However, since their ability to self-support dissipates with growth, they need additional support in order to ascend to the canopy and thrive in mature forests (Gentry 1991; Gerwing et al. 2006). Most lianas show cambial variants that are variations of cambial conformations, products and number. The most common condition in woody species is a single and cylindrical cambium, which produces secondary xylem (internally) and secondary phloem (externally) with similar amounts around stem circumference (Carlquist 2001). Some species of lianas do not show cambial variants (Carlquist 1991, 2001; Caballe 1993), but frequently, such lianas do show wood

anatomical tendencies correlated to the habit, e.g., wide vessels, higher conductive area, low proportion of supportive tissues, and high amount of parenchyma (Brandes and Barros 2008; Carlquist 1991). Only a few papers have reported the growth ring anatomy of lianas (Baas and Schweingruber 1987; Carlquist 1995; Gasson and Dobbins 1991; Lima et al. 2010; Schweingruber 2007). Leguminosae are the third largest family of climbers in the New World. Additionally, along with Bignoniaceae, they represent the dominant climbing families in Neotropical lowland forests (Gentry 1991). Lianas compete with trees for nutrients, light and water (Gentry 1991). As a consequence of their thin stems and low-density wood, lianas capture less carbon than tree species. Moreover, infestations of lianas inhibit the regeneration of forest trees which also reduces the amount of carbon that would otherwise be assimilated in the biomass (Schnitzer and Bongers 2002). In this study, we analyzed eight liana species from a well-preserved remnant of the Atlantic Forest located in a mountainous region (Serra da MantiqueiraItatiaia Massif). These species represent almost all legume lianas previously recorded in this place and registered in the Programa Mata Atlantica database. In the course of our study, we asked (1) if Atlantic Forest lianas have growth rings, (2) what anatomical features distinguish such growth rings, (3) what periodicity applies to the formation of growth rings, and (4) whether ring-width patterns reect precipitation variations.

Materials and methods Study site The samples were collected from the Parque Nacional do Itatiaia, municipality of Itatiaia, State of Rio de Janeiro, southeastern Brazil. The park is located between the geographical coordinates of 22150 22300 S and 44300 44450 W, with an area of 28,155.97 ha (Morim 2006). Its type of vegetation can be classied as Atlantic Forest (Oliveira-Filho and Fontes 2000). Most of the Parque Nacional do Itatiaia lies in a mountainous area with several well-delimited climatic and vegetation belts related to altitudinal gradients. The samples were taken between 700 and 1,100 m elevation. At 816 m elevation, the annual mean precipitation is around 1,700 mm, and the annual mean temperature is 18.2C. The warm and rainy season is between December and February, when 50% of the annual precipitation occurs. January is the rainiest month, with a mean of 290 mm. During these months, the mean temperature is 20.8C. The dry cold season is between June and August, with only 5% of the annual precipitation. The driest month is June, with a mean of 32 mm. During these months, the mean temperature is 15.1C, but an absolute

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minimum of 0C has been registered (Segadas-Vianna and Dau 1965). The precipitation data used in our dendrochronological analysis were collected during 19862005 at the meteorological station of Resende (22 270 S, 44 260 W) and were provided by the Instituto Nacional de Meteorologia (INMET) (National Institute of Meteorology)Sixth Meteorological District (Fig. 1). The meteorological station of Resende is 453 m elevation, around 18 km distance from study site, and the precipitation data are very similar of study site (Segadas-Vianna and Dau 1965). Wood anatomy We sampled 57 lianas from eight Leguminosae species (subfamilies Mimosoideae and Papilionoideae). Of these, four had cambial variants and four did not. The cambial variants that occur in these species are the non-fragmented
300 150 125 100 75 50 25 0
JAN FEB JUL APR SEP JUN MAY AUG OCT MAR NOV DEC

Precipitation (mm)

200 150 100 50 0

Fig. 1 Mean (19862005) monthly precipitation (bars) and temperature (line) for Resende-RJ Meteorological Station

Table 1 Studied species, anatomical features of the growth rings, cambial variant types, analyzed samples RBw Species Mimosoideae Senegalia grandistipula Senegalia lacerans Senegalia martiusiana Senegalia pedicellata Senegalia tenuifolia Piptadenia adiantoides Piptadenia micracantha Papilionoideae Dalbergia frutescens 1, 2, 3a, 4a Absent 8,606, 8,613, 8,614, 8,616, 8,617, 8,618, 8,619, 8,620, 8,621, 8,622, 8,623, 8,626, 8,630, 8,633, 8,649 1a, 3a, 4a, 5a 1a, 2a, 3a, 4a, 5a 1a, 3a, 5a 1a, 3a, 5a 1, 2, 3a, 4a 1a, 2, 3a, 4 1, 2, 3, 4
a

Anatomical features of growth rings

Temperature ( C)

250

lobed stem and the xylem-furrowed stem (Brandes and Barros 2008) (Table 1). Both are products of a single cambium with unequal activity on some regions (Carlquist 2001). For this study, we selected lianas larger than 2.0 cm in diameter at approximately 1.3 m above the ground, without wounds or deformations at this height. The number of samples per species differed because of the difculty in nding individuals with the characteristics cited above and the different abundance of each species. For each individual sampled, a voucher was collected, representing reproductive and other vegetative parts as well. They were stored at the herbarium Jardim Botanico do Rio de Janeiro (RB). Wood samples of the stems were collected at approximately 1.3 m above the ground. We collected partial or complete cross-sections, including bark, wood and pith. Blocks were polished for macroscopic observation through an Olympus SZ11 stereomicroscope. The images were taken by a photographic camera (Olympus C5050) attached to the same stereomicroscope and analyzed with Image Pro Plus version 3.0 for Windows. For light microscopy, boiling water and glycerine were used to soften part of the blocks; 12 to 30 lm-thick sections were made in transversal, tangential and radial plains, using a Spencer 860 sliding microtome. After cleaning, they were stained with safranin and astra blue (Bukatsch 1972), dehydrated, and mounted on Permount resin in permanent slides. Slides were observed using an Olympus BX50 microscope, and images were captured with Image Pro Plus version 3.0 for Windows linked to the microscope through a Media Cybernetics CoolSNAP-Pro video camera. The Zeiss

Cambial variants

Samples RBw

Lobed stem Xylem furrowed Lobed stem Lobed stem Absent Absent Absent

8,627, 8,643, 8,644 8,607, 8,608, 8,610, 8,611, 8,612, 8,624, 8,625, 8,629, 8,631, 8,641, 8,642 8,653, 8,655, 8,656, 8,657, 8,659, 8,660, 8,661 8,609, 8,615, 8,662, 8,663, 8,664 8,628, 8,658 8,634, 8,635, 8,636, 8,646, 8,647, 8,648, 8,652 8,605, 8,632, 8,637, 8,645, 8,650, 8,651, 8,654

1 semi-ring-porous, 2 marginal parenchyma, 3 ber zone, 4 radially attened latewood cells, 5 pith eck and traumatic canals
a

Features not present in all growth rings

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polarized light microscope with red lter k was also used to observe calcium oxalate crystals. Wood samples and permanent slides were incorporated into the wood collection from the Jardim Botanico do Rio de Janeiro (RBw). The terminology complies with the IAWA Committee (1989). Cambial wounding The technique of repeated wounding of the vascular cambium, the so-called Mariaux Window (Mariaux 1967), was used to analyze the characteristics of the secondary xylem produced during the year, as well as conrm the presence of annual growth rings. In the procedure, the bark and the cambium at 0.5 cm in width and approximately 5 cm in height were removed, and a Bordeaux mixture was applied to avoid the action of pathogenic microorganisms. Four markings were performed throughout the year (one in each season), and 1 year after the rst wound, a section of the area appointed for analysis was collected. Fifteen individuals of Dalbergia frutescens, seven Piptadenia adiantoides, seven Piptadenia micracantha, and two Senegalia tenuifolia were analyzed. Dendrochronology For dendrochronological studies, samples of 29 lianas from Piptadenia adiantoides, Piptadenia micracantha, and Dalbergia frutescens species were analyzed (Table 2). Senegalia tenuifolia, one species that shows a distinctive growth ring, was not used because we could not nd enough specimens to study. Four rays (temporal series) were measured per liana. Growth ring measurements and image processing were performed with Image Pro Plus version 3.0 for Windows, with a precision of 0.01 mm. The cross-dating of the temporal series was performed, following the recommendations of Stokes and Smiley (1996) and Fritts (1976) and was supported by graphs and statistical analysis. The
Table 2 Ring-width data Chronology Mimosoideae Piptadenia adiantoides Piptadenia micracantha Papilionoideae Dalbergia frutescens 15 (15) 60 (37) 0.50 0.51 7 (7) 7 (6) 28 (21) 28 (14) 0.69 0.48 0.57 0.37

COFECHA (Holmes 1983) program was used to verify the precision of the measurements and the cross-dating. The growth ring series was standardized (de-trended) using a spline curve (cubic smoothing spline 50% wavelength cutoff; 5 years rigidity of spline for ltering). A exible spline was used to minimize undesirable signal (e.g., competition and local disturbance). The exible spline is an appropriate de-trending method for trees from closed-canopy stands, as previously reported (Brienen and Zuidema 2005; Cook and Peters 1981), and it may also be applicable to lianas, taking into account ecological conditions. For each of these species, a reference, or master, chronology was produced, calculating the mean value of all standardized series (de-trended series). Each temporal series was tested in relation to the reference chronology. A nal growth ring chronology was produced for each species by averaging the best correlated series. Successful cross-dating indicates the inuence of an external growth factor on tree growth in a region. By identifying the common signal that represents the climatic factor in a growth rings time series, it is possible to retain the highly correlated series in the nal chronologies. Finally, a mean reference chronology (master chronology) of lianas from the Parque Nacional de Itatiaia was produced from the species chronologies. For the time series analysis and building the chronologies, software from the Dendrochronology Program Library (Holmes 1994) was used. Pearson correlation analyses were performed between the chronologies produced and annual precipitation (JanuaryDecember), monthly precipitation and the precipitation total of DecemberJanuaryFebruary (summer), March AprilMay (autumn), JuneJulyAugust (winter), and SeptemberOctoberNovember (spring). The correlation analyses were executed using Statistica 8.0 software. Correlation analysis is also the most common method to measure the association between growth rings and climate (Fritts 1976). The methods described above for the treatment and analysis of data are an attempt to follow the

Number Number Intercorrelation Sensitivity Chronology Samples RBw of lianas of series extension

19932005 8,634, 8,635, 8,636, 8,646, 8,647, 8,648, 8,652 19872005 8,605, 8,632, 8,637, 8,645, 8,650, 8,651, 8,654

19702005 8,606, 8,613, 8,614, 8,616, 8,617, 8,618, 8,619, 8,620, 8,621, 8,622, 8,623, 8,626, 8,630, 8,633, 8,649

Species, number of lianas before and after cross-dating (), number of series before and after cross-dating (), intercorrelation, sensitivity, chronology extension, and analyzed samples RBw

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methodological steps recommended by Braker (2002) which visualize, explore, test, and relate data.

Results Wood anatomy Distinct growth rings were observed in all studied species. The four species without cambial variants revealed easily detectable and well-delimited growth rings (Figs. 2ad, 3ad). Anatomical ring boundaries of species with cambial variants were sometimes detectable, sometimes barely detectable rings or even undetectable (Figs. 4ad, 5ad). The most evident anatomical features of growth rings were semi-ring porosity, brous zones, marginal parenchyma bands, and radially attened latewood cells. Species with cambial variants also exhibited traumatic canals and pith ecks within the growth boundaries. The features listed above were not present concomitantly in all growth rings

(Table 1). In combination, the macroscopic and microscopic observations enabled a proper distinction of growth rings. Usually, the macroscopic view facilitated the detection of growth ring boundaries because of a broader eld view. Among the species without cambial variants, Dalbergia frutescens (Vell.) Britton var. frutescens (subfamiliy Papillionideae) (Figs. 2a, 3d), P. adiantoides (Spreng.) J. F. Macbr. (Figs. 2b, 3b), P. micracantha Benth. (Figs. 2c, 3c) and Senegalia tenuifolia (L.) Britton and Rose (subfamily Mimosoideae) (Figs. 2d, 3a) exhibited semi-ring porosity, marginal parenchyma, brous zones in latewood, and radially attened latewood cells. However, a brous zone and radially attened latewood cells were not present in all growth rings of D. frutescens (Figs. 2a, 3d) and S. tenuifolia (Figs. 2d, 3a). Within P. adiantoides (Figs. 2b, 3b) some growth rings did not present semi-ring porosity and ber zone. In P. micracantha (Figs. 2c, 3c) few growth rings showed radially attened latewood cells. Abundance of prismatic calcium oxalate crystals was observed near growth ring boundaries of all Mimosoideae without cambial variants. The other studied species of genus Senegalia revealed cambial variants. Although all species exhibit distinct growth ring boundaries, they are sometimes difcult to detect or, in some stem portions, even undetectable. The main distinctive features of growth rings for this genus included semi-ring porosity and brous zone. S. grandistipula (Benth.) Seigler and Ebinger revealed a square-like lobed stem cambial variant. In addition to the features mentioned above, some growth rings had radially attened latewood cells, pith ecks and traumatic canals (Figs. 4a, 5a). S. lacerans (Benth.) Seigler and Ebinger showed a xylem-furrowed cambial variant. Beyond the features for genus, some growth rings had marginal parenchyma, radially attened latewood cells, pith ecks and traumatic canals (Figs. 4c, 5b). S. martiusiana (Steud.) Seigler and Ebinger, a lobed stem cambial variant with cylindrical lobes, presented the features cited above for the genus, including pith ecks and traumatic canals (Figs. 4d, 5c). Finally, S. pedicellata (Benth.) Seigler and Ebinger, a lobed stem cambial variant with attened lobes, showed pith ecks and traumatic canals (Figs. 4b, 5d). Occasionally, semi-ring porosity and brous zone were also presented. Cambial wounding The four studied species showed a clear periodicity in radial growth, with the formation of one growth ring per year. At the beginning of the rainy season in September, the cambium produced large vessels. As the dry season approached, vessels with gradually smaller diameters were

Fig. 2 Transverse sections (light microscopy) of a D. frutescens, b P. adiantoides, c P. micracantha, d S. tenuifolia. Arrows indicate growth ring boundaries, scale bars 100 lm

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138 Fig. 3 Transverse sections (stereomicroscopy) of a S. tenuifolia, b P. adiantoides, c P. micracantha, d D. frutescens. Arrows indicate growth ring boundaries, scale bars 1 mm

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period; however, we noticed that the products of the vascular cambium (cells composing the secondary xylem) and the size of these cells varied throughout the year. Dendroecology All studied species included discontinuous rings (wedging rings), which may cause serious difculties for proper synchronization between tree-ring series. Since we mainly used complete or partial sections of liana stems and not samples collected with an increment borer, it was possible to validate the cross-dating of radii and to identify discontinuous rings with a certain ease and precision. Both, graphical analysis and statistics provided by COFECHA software were very important to synchronize the measured growth ring series. Thus, the cross-dating procedure was successful between most radii and individuals, as indicated by a high intercorrelation between the tree-ring series of 0.69 for P. adiantoides, 0.50 for D. frutescens and 0.48 for P. micracantha (Table 2), for which three growth ring chronologies were produced (Fig. 7). The mean sensitivity was 0.57 in P. adiantoides, 0.51 in D. frutescens and 0.37 in P. micracantha (Table 2), revealing a high inter-annual growth variability that might be related to climate sensitivity (Fritts 1976). Finally, a mean chronology of lianas from Itatiaia was built by averaging the three individual species chronologies (Fig. 7d). Correlation analysis between the individual species chronologies and total annual precipitation revealed signicant correlation coefcients for D. frutescens (r = 0.63; p = 0.003), P. adiantoides (r = 0.53; p = 0.062) and P. micracantha (r = 0.39; p = 0.096), respectively. The correlation between the mean chronology of lianas from Itatiaia and total annual precipitation was even higher than

Fig. 4 Transverse sections (light microscopy) of a S. grandistipula, b S. pedicellata, c S. lacerans, d S. martiusiana. Arrows indicate growth ring boundaries, scale bars 100 lm

produced (Fig. 6ad). Through the experimental delineation employed, it was not possible to determine whether the vascular cambium became inactive for a determined

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Trees (2011) 25:133144 Fig. 5 Transverse sections (stereomicroscopy) of a S. grandistipula, b S. lacerans, c S. martiusiana, d S. pedicellata. Arrows indicate growth ring boundaries, scale bars 1 mm

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that found for the individual species (r = 0.66; p = 0.001) (Table 3, Fig. 7). Highest correlation coefcients of the chronologies with monthly and seasonal precipitation were generally observed for the summer months of the previous growing season and the spring months of the current growing season. Lowest correlations were observed for autumn and winter, except for P. micracantha. The P. adiantoides chronology was signicantly correlated with precipitation of February of the previous growing season, October of the current season, and summer of the previous growing season (Table 3). For D. frutescens, positive correlations occurred with January of the previous growing season, September of the current season, and summer of the previous growing season. In contrast to these species, growth of P. micracantha was positively correlated with June and July of the previous growing season, winter of the previous growing season and May of the current growing season (Table 3, Fig. 7).

Discussion and conclusions The anatomical results demonstrate that P. micracantha, P. adiantoides, S. tenuifolia and D. frutescens form clear annual rings, which is fundamental for precise ring counting and ring-width measurements. In contrast, Senegalia grandistipula, S. lacerans, S. martiusiana and S. pedicellata are species with cambial variants that may form distinct growth rings, which are sometimes indistinct and difcult to detect or absent in some stem portions. Beyond that, species which show lobate growth should not be used in an analysis of growth rings (Worbes 1989). Growth rings were detected in

other liana species, but they were rarely analyzed in detail. Baas and Schweingruber (1987) observed that climbers from temperate climates show ring porous and semi-ring porous wood anatomy. Other examples of lianas with distinct growth rings from temperate and tropical regions were presented by Schweingruber (2007). Gasson and Dobbins (1991) report distinct growth rings in lianas from the genera Capsis, Schlegelia nine other genera of the Bignociaceae family. A detailed description of growth rings in tropical lianas from the Bignonieae tribe was provided by Lima et al. (2010). In lianas from Venezuela, growth rings marked by marginal parenchyma were observed in Anomospermun schomburgkii Miers (Menispermaceae) and Strycnos brachistantha Standley (Loganiaceae) (Araque et al. 2000). The main anatomical markers for growth rings observed by these authors were semi-ring porosity, parenchyma bands, radially attened latewood bers and radially shorter ray cells. Semi-ring porosity and marginal parenchyma were also important features observed in the present study. They were present in all studied species without cambial variants and having a distinct growth ring. These studies show that growth rings in lianas are not exceptional and have common anatomical features. Based on the evidence from wood anatomy, vascular cambium wounds (Worbes 1995), cross-dating, intercorrelation between ring-width time series, correlations between chronologies and precipitation data (Stahle 1999), as well as the seasonal rainfall regime of the study area, we conclude that growth rings of the studied species are formed annually. According to Worbes (1995), areas with a dry season of 3 months or more with a monthly precipitation below 60 mm are favorable for the occurrence of species that form annual growth rings. This holds true for

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Fig. 6 Macroscopic cross-sections of cambial wounds set in December 2005. Collection of the samples was conducted after 1 year (December 2006). a S. tenuifolia, b P. adiantoides, c P. micracantha, d D. frutescens. Scale bars 1 mm

the Parque Nacional do Itatiaia, where the dry season lasts 3 months. Supporting this evidence, Schweingruber (2007) reported growth rings in tropical lianas from seasonal climates. The occurrence of annual growth rings and annual growth seasonality was also reported in arboreal species from the Atlantic Forest (Callado et al. 2001b; Estrada et al. 2008; Lisi et al. 2008; Oliveira et al. 2009, 2010), in lianas from the Atlantic Forest of the Bignoniaceae family (Lima et al. 2010) and in lianas of the Leguminosae from a Mexican tropical rainforest (Leon-Gomez and Monroy-Ata 2005).

The successful cross-dating and the high intercorrelation values between ring-width series showed that liana species of this study share a common growth pattern and respond to a common environmental signal. Importantly, the dendrochronological results suggest that the growth of tropical lianas is sensitive to variations in local climate. Specically, positive correlations between the chronologies and annual, monthly and seasonal precipitation were observed. Strongest relationships were observed between chronologies and annual precipitation. Precipitation was also reported as the most important factor for the secondary growth of tropical tree species (Worbes 1989). Schongart et al. (2006) studied six arboreal species in Africa, among them four species of the Leguminosae family and observed signicant correlations (p \ 0.01) between growth rates and annual precipitation. In a tropical dry forest in Costa Rica, Enquist and Lefer (2001) observed a signicant relationship between growth of the evergreen Capparis indica and annual precipitation. Fichtler et al. (2004) studied two leguminous species from a semiarid forest in Namibia and found a positive relationship between a Burkea africana chronology and the rainfall total of all months to the growth year (AugustJuly). Worbes (1999) studied several species in Venezuela and detected a high correlation coefcient (r = 0.75; p \ 0.05) of annual precipitation with the mean chronology of all studied species. Besides, signicant correlations of 0.62 (p \ 0.05) and 0.68 (p \ 0.05) between chronologies of Cedrela odorata and Terminalia guianensis and annual rainfall were found. Similar to these reports, the present study demonstrates that a mean chronology of several species shows a higher relationship to annual precipitation than chronologies of individual species. Climate during certain periods of the year may have a greater inuence on growth than during other periods (Fritts 1976). For example, D. frutescens and P. adiantoides show signicant correlations with precipitation during summer of the previous growing season and with some spring months of the current growing season. On the other hand, P. micracantha shows signicant correlations with precipitation in winter of the previous growing season. Thus, in some of the studies noted above, a controversial picture arises with correlation between growth and precipitation between dry and rainy seasons, as well as with transitional months. Brienen and Zuidema (2005) related tree growth in a Bolivian rain forest with rainfall. While they did not nd any correlation between chronologies and annual precipitation, they documented a positive relationship between tree growth and precipitation during certain periods of the year. Three species showed a relationship to precipitation at the beginning of the rainy season, one species with precipitation in the transition from the rainy to the dry

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D. frutescens Total annual precipitation P. adiantoides February precipitation

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a
Indexed ring width

2 1

2500

b
Precipitation (mm) Indexed ring width

2000 0
-1 -2

1 0
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350 250 150 50

1500 1000

-3 -4 40 30 20 10 0 1970 1972 1974 1976 1978 1980 1982 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004

Sampling depth

Sampling depth

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30 20 10 0
1970 1972 1974 1976 1978 1980 1982 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004

Year
P. micracantha Winter precipitation Lianas Itatiaia

Year
Total annual precipitation

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Indexed ring width

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d
Precipitation (mm) Indexed ring width

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2500 2000

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0 -1 -2 1000 -3 -4 80 60 40 20 0
1970 1972 1974 1976 1978 1980 1982 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004

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20 10 0
1970 1972 1974 1976 1978 1980 1982 1984 1986 1988 1990 1992 1994 1996 1998 2000 2002 2004

Year

Sampling depth

500

Year

Fig. 7 Ring-width chronologies and their sampling depth and comparison with precipitation. a D. frutescens and total annual precipitation, b P. adiantoides and February precipitation,

c P. micracantha and winter precipitation, d Mean chronology of lianas from Itatiaia and total annual precipitation

season, and two species were correlated with precipitation in the transition period from dry to rainy. Dunisch et al. (2003) observed the highest correlation coefcients of Swietenia macrophylla with rainfall in November, December, January and May, and in Cedrela odorata in March, April and May, and rainy months of the previous growth period. Fichtler et al. (2004) studied the leguminous trees Burkea africana and Pterocarpus angolensis in Namibia. P. angolensis from Katima Mulilo was highly correlated to rainfall in April and total precipitation of April and May, the beginning of the dry season. The chronology B. africana from Ondangwa responded to rainfall in January and February, the rainy season, and the chronology from Katima Mulilo responded to rainfall of August, September and November, the end of dry season, as well as the total rainfall for October and November, the beginning of the rainy season. Eshete and Stahl (1999)

observed high correlations in Acacia species with precipitation total from June to September, the rainy season. In Venezuela, Worbes (1999) noticed signicant correlations between dry season precipitation and ve species and between rainy season precipitation and four species studied. Two of these species showed correlations with both the dry season and rainy season rainfall. Enquist and Lefer (2001) noticed correlations of growth of Genipa americana with the precipitation of the dry season and of Capparis indica with the rainy season of the previous year. The different reaction pattern of the two species is explained by individualistic response and differences in the root system. Regarding lianas, Lima et al. (2010) detect cambial activity in Tynanthus cognatus (Bignoniaceae) only at the end of the rainy season. To summarize, precipitation is an important climatic factor related to the growth of woody species in the tropics, being it trees or lianas. Moreover, it

Precipitation (mm)

Precipitation (mm)

450

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Table 3 Correlation coefcients between chronologies and monthly precipitation (JanAug previous growing season; SepJun current growing season), total precipitation in summer (SUM), autumn (AUT), winter (WIN), spring (SPR) and total annual precipitation (TAP) Previous growing season Jan Piptadenia adiantoides Piptadenia micracantha Dalbergia frutescens Lianas Itatiaia 0.33 0.36 0.51 0.56 Feb 0.57 0.12 0.37 0.31 Mar -0.18 0.14 -0.06 -0.03 Apr -0.21 0.27 0.11 0.21 May 0.11 -0.24 0.30 0.06 Jun -0.24 0.56 0.05 0.32 Jul 0.34 0.52 -0.01 0.31 Aug -0.12 -0.16 -0.41 -0.36

Current growing season Sep Piptadenia adiantoides Dalbergia frutescens Lianas Itatiaia 0.32 0.55 0.49 Oct Nov Dec Jan Feb Mar 0.43 Apr May Jun SUM AUT -0.21 0.25 0.15 WIN 0.04 SPR TAP

0.53 -0.21 0.42 -0.24 -0.28 0.11 0.01 0.22 0.00 -0.18 -0.28 0.05 0.17 -0.37 -0.34

0.50 -0.32 0.07

0.11 0.52

0.28 0.53 0.38 0.63 0.21 0.66

Piptadenia micracantha 0.17 -0.44 -0.06 0.34 -0.32 -0.30 -0.03

0.45 -0.41 0.13 0.25 0.50

0.54 -0.17 0.39 0.12

0.32 -0.11 -0.57 -0.01 0.58 0.24 -0.02 -0.16

0.12 -0.25

Signicant correlations: Italic value p \ 0.08; Bold value p \ 0.05; Bold italic value p \ 0.005

appears that growth can be related to precipitation of either a short period (seasons or months) or a long period (year). In an interesting study about the abundance patterns of lianas, Schnitzer (2005) found that lianas are more abundant in dry seasonal forests. He suggested that lianas can maintain their growth activity during the dry season, by gathering enough water resources with their deep roots to continue their photosynthesis and growth. Thus, lianas confer an adaptive advantage over trees. This communitylevel explanation can be supported by our results for P. micracantha. At the same time, however, the present study shows that the growth of D. frutescens and P. adiantoides is conned mostly to the rainy season. These results corroborate Enquist and Lefers (2001) hypothesis of individualistic response to climate, as well as the idea that some tropical assemblages may in fact be structured by species-specic differences in soilwater use. It is possible that lianas respond well to precipitation variations, as a result of their peculiarities regarding the conduction of sap in the xylem. In lianas, vessels of large diameter are a common feature (Carlquist 1985; Ewers et al. 1990; Ewers et al. 1991), which is also a characteristic in the species of this study (Brandes and Barros 2008). The large liana vessels are more susceptible to embolism during the dry season than vessels of smaller diameter (Zimmermann 1983). During the dry season, droughtsensitive species show a reduction in their growth in comparison with drought-tolerant species, and in the rainy season, they show an increase in growth. Thus, it is expected that drought-sensitive species show a better

correlation with climatic parameters, especially during the rainy season (Gebrekirstos et al. 2008). While precipitation is an important factor for the secondary growth of liana species, other environmental factors, such as temperature, solar radiation, day length and phenological phases, may also inuence the formation of growth rings (Callado et al. 2001b; Clark and Clark 1994; Devall et al. 1995; Oliveira et al. 2009, 2010; Schweingruber 2007). Their relevance for controlling growth rings in lianas has to be tested in further studies. In this study, wedging rings were detected in all species during the cross-dating procedure of time series of radial growth series within individuals. The analysis of stem discs facilitated the detection of problematic growth rings (Worbes 1999). Absent and wedging rings may lead to age underestimation and hence growth overestimation (Lorimer et al. 1999). The presence of wedging rings was reported from several neotropical arboreal species, and it was observed that they are more common in small understory trees growing under competition with diminished light conditions (Lorimer et al. 1999; Worbes 2002). Ecological studies on lianas report a strong competition pressure with trees for nutrients, light, and water during the dry season (Schnitzer and Bongers 2002). The presence of wedging rings documented in our study reinforces the idea that lianas are subject to competition processes which may initiate alterations of cambial activity in determined stem regions. Thus, we conclude that the lianas studied do have growth rings, detectable by wood anatomical features like semi-ring

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143 Callado CH, Neto SJS, Scarano FR, Costa CG (2004) Radial growth dynamics of Tabebuia umbellata (Bignoniaceae), a ood-tolerant trees from the Atlantic forest swamps in Brazil. IAWA J 25:175183 Carlquist S (1985) Observations on functional wood histology of vines and lianas: vessel dimorphism, tracheids, vasicentric tracheids, narrow vessels, and parenchyma. Aliso 11:139157 Carlquist S (1991) Anatomy of vine and liana stems: a review and synthesis. In: Putz FE, Mooney HA (eds) The biology of vines. Cambridge University Press, Cambridge, pp 5372 Carlquist S (1995) Wood and bark anatomy of Ranunculaceae (including Hydrastis) and Glaucidiaceae. Aliso 14:6584 Carlquist S (2001) Comparative wood anatomy: systematic, ecological and evolutionary aspects of dicotyledon wood, 2nd edn. Springer-Verlag, Berlin Clark DA, Clark DB (1994) Climate-induced annual variation in canopy tree growth in a Costa Rican tropical rain forest. J Ecol 82:865872 Committee IAWA (1989) List of microscopic features of hardwood identication. IAWA Bull N. ser. 10:219332 Cook ER, Peters K (1981) The smoothing spline: a new approach to standardizing forest interior tree-ring width series for dendroclimatic studies. Tree-ring Bull 41:4553 Devall MS, Parresol BR, Wright SJ (1995) Dendroecological analysis of Cordia alliodora, Pseudobombax septenatum and Annona spraguei in central Panama. IAWA J 16:411424 Dunisch O, Montoia VR, Bauch J (2003) Dendroecological investigations on Swietenia macrophylla King and Cedrela odorata L. (Meliaceae) in the central Amazon. Trees 17:244250 Eckstein D, Baas P (1999) Dendrochronology in Monsoon Asia. IAWA J 20:223350 Eckstein D, Sass U, Baas P (1995) Growth periodicity in tropical trees. IAWA J 16:323442 Enquist BJ, Lefer AJ (2001) Long-term tree ring chronologies from sympatric tropical dry-forest trees: individualistic responses to climatic variation. J Trop Ecol 17:4160 Eshete G, Stahl G (1999) Tree rings as indicators of growth periodicity of acacias in the Rift Valley of Ethiopia. For Ecol Manag 116:107117 Estrada GCD, Callado CH, Soares MLG, Lisi CS (2008) Annual growth rings in the mangrove Laguncularia racemosa (Combretaceae). Trees 22:663670 Ewers FW, Fisher JB, Chiu ST (1990) A survey if vessel dimensions in stem of tropical lianas and others growth forms. Oecologia 84:544552 Ewers FW, Fisher JB, Fichtner K (1991) Water ux and xylem structure in vines. In: Putz FE, Mooney HA (eds) The biology of vines. Cambridge University Press, Cambridge, pp 127160 Fichtler E, Trouet V, Beeckman H, Coppin P, Worbes M (2004) Climatic signal in tree rings of Burkea africana and Pterocarpus angolensis from semiarid forest in Namibia. Trees 18:442451 Fritts HC (1976) Tree rings and climate. The Blackburn press, New Jersey Gar G, Ficarrotta S (2003) Inuence of ivy (Hedera helix L.) on the growth of downy oak (Quercus pubescens s.l.) in the Monte Carcaci Nature Reserve (central-western Sicily). Ecol Mediter 29:514 Gasson P, Dobbins DR (1991) Wood anatomy of the Bignoniaceae, with a comparison of trees and lianas. IAWA Bull 12:389417 Gebrekirstos A, Mitlohner R, Teketay D, Worbes M (2008) Climate growth relationships of the dominant tree species from semi-arid savanna woodland in Ethiopia. Trees 22:631641 Gentry AH (1991) The distribution and evolution of climbing plants. In: Putz FE, Mooney HA (eds) The biology of vines. Cambridge University Press, Cambridge, pp 350

porosity, brous zone, marginal parenchyma and radially attened latewood cells. The four species without cambial variants had well-delimited growth rings, which were easily detectable. The periodicity of growth ring formation and correlation of ring-width time series proved the annual nature of their growth rings. Climate-growth analyses revealed that growth is conditioned by precipitation. Future ecological studies, particularly dendroecological studies, will be an important source of information about the role played by lianas in the Atlantic Forest of Brazil and in other tropical forest ecosystems.
Acknowledgments Our thanks go to the Instituto de Pesquisas Jardim Botanico do Rio de Janeiro, Petrobras and CAPES (Coorde nacao de Aperfeicoamento de Pessoal de Nvel Superior) for nancial support; Parque Nacional do Itatiaia for logistical support and Dr. Achim Braeuning for the revision of the paper and valuable suggestions and comments.

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